Silent gene clusters encode magnetic organelle biosynthesis in a non-magnetotactic phototrophic bacterium

Horizontal gene transfer is a powerful source of innovations in prokaryotes that can affect almost any cellular system, including microbial organelles. The formation of magnetosomes, one of the most sophisticated microbial mineral-containing organelles synthesized by magnetotactic bacteria for magnetic navigation in the environment, was also shown to be a horizontally transferrable trait. However, the mechanisms determining the fate of such genes in new hosts are not well understood, since non-adaptive gene acquisitions are typically rapidly lost and become unavailable for observation. This likely explains why gene clusters encoding magnetosome biosynthesis have never been observed in non-magnetotactic bacteria. Here, we report the first discovery of a horizontally inherited dormant gene clusters encoding biosynthesis of magnetosomes in a non-magnetotactic phototrophic bacterium Rhodovastum atsumiense. We show that these clusters were inactivated through transcriptional silencing and antisense RNA regulation, but retain functionality, as several genes were able to complement the orthologous deletions in a remotely related magnetotactic bacterium. The laboratory transfer of foreign magnetosome genes to R. atsumiense was found to endow the strain with magnetosome biosynthesis, but strong negative selection led to rapid loss of this trait upon subcultivation, highlighting the trait instability in this organism. Our results provide insight into the horizontal dissemination of gene clusters encoding complex prokaryotic organelles and illuminate the potential mechanisms of their genomic preservation in a dormant state.